What Have Pesticides Got to Do with It?
Maryann Frazier, Chris Mullin, Jim Frazier and Sara Ashcraft
Department of Entomology; Penn State University, 501 ASI Building, University Park, PA
There is agreement among beekeepers and scientists that the health of honey bees has been in
decline for years, and the rate of decline appears to be accelerating. A 2007 survey estimated a
loss of about 1/3 of US honey bee colonies during the winter of ’06-’07 (vanEngelsdorp et al.
2007). It is generally agreed that varroa mites are playing a key role in the demise of honey bee
health; additionally, the interaction between diseases and varroa and the newly identified Israeli
acute paralysis virus (IAPV) are likely important contributing factors (Cox-Foster et al., 2007).
However, the past year’s research into the newest malady, Colony Collapse Disorder (CCD),
supports an emerging hypothesis that no one factor alone is responsible for the dramatic losses of
honey bees in general or CCD specifically.
A 2007 publication by the National Academy of Sciences documents a decline in many North
American pollinators (Committee on the Status of Pollinators in North America, 2007). Another
study published in the journal Science documented a loss not only of pollinators in Great Britain
and the Netherlands, but also in the plants that are dependent on them for pollination (Biesmeijer
et al. 2006). Clearly the phenomenon of pollinator decline is not limited to honey bees or to the
US and the consequences are far reaching for agriculture and our food supply.
Are pesticides a contributing factor?
Honey bee exposure to chemical pesticides has long been a concern for beekeepers and growers
alike. A large portion of our 2.4 million colonies is utilized for crop pollination and typically
employed on several different crops per season. These colonies are at risk of exposure to the
pesticides used by growers to control pest insects, diseases and weeds. Also, our own use of
miticides within the hive to control varroa mites has long been a concern due to their potential
impacts on developing bees (especially queens) and contamination of hive products. In the past,
pesticide poisoning of honey bees has been associated with lethal exposure and the obvious
symptom of a pile of dead bees in front of the hive. We are becoming increasingly concerned
that pesticides may affect bees at sublethal levels, not killing them outright, but rather impairing
their behaviors or their ability to fight off infections. For example, pesticides at sublethal levels
have been shown to impair the learning abilities of honey bees or to suppress their immune
systems (Desneuz et al. 2007). For these reasons we believe that pesticide exposure may be one
of the factors contributing to pollinator decline and CCD.
The prevalence of pesticides
In 2007 we analyzed pollen (bee bread and trapped pollen) and wax for pesticide residues. A
significant number of samples analyzed were from operations impacted by CCD and control
operations (not impacted by CCD) that were collected by members of the CCD working group as
a part of a larger CCD study (the results of which will be published at a later date). Additional
samples were from honey bee colonies placed in Pennsylvania apple orchards where pesticide
applications over the past 7 years have been well documented. The third source was from
beekeepers, who trapped pollen while their bees were in specific cropping situations or who were
concerned about the declining health of their colonies. Samples were mainly from migratory
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operations but also included smaller, non-migratory operations and the PSU research apiaries,
with operations represented from across the country. The USDA Agricultural Marketing
Service, National Science Laboratory in Gastonia, NC, conducted the pesticide residue analysis
under the direction of chemist Roger Simonds, who is also a beekeeper. The pollen samples were
analyzed for 171 chemicals, and some metabolites. Metabolites are the breakdown products of
pesticides, and some can be more toxic than their parent compound. Wax samples were similarly
analyzed.
In a total of 108 pollen samples analyzed, 46 different pesticides including six of their
metabolites were identified. Figure 1 summarizes the pesticide classes found and the number of
different pesticides identified within each class. Up to 17 different pesticides were found in a
single sample. Samples contained an average of 5 different pesticide residues each. Only three
of the 108 pollen samples had no detectable pesticides. Figure 2 shows the 14 most frequently
detected pesticide residues in pollen and the percentage of samples containing them.
Figure 1. Pesticide class and types of compounds detected in 108 pollen samples in 2007.
Insecticide
Metabolites
6
Herbicides
6
Insecticid
es
Fungicides
14
Pyrethroids
4
5
Organophosphates
3
3
8
Carbamates
Neonicotinoids
Insect Growth Regulators
Organochlorines
1
2
Chlorinated Cyclodienes
100
90
80
70
60
50
40
30
20
10
0
Fl
uv
al
in
at
e
Co
um
ap
ho
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lo
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y
do
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n
(T
ot
al
)
A
tra
z
in
Fe
e
np
ro
pa
th
Ch
rin
lo
r
o
Cy
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al
ha
on
lo
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rin
(T
ot
al
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)
et
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e
Percent Frequency (%)
Figure 2. Most frequently detected pesticides in honey bee pollen (bee bread and trapped at
entrances).
Pesticides
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Some samples had multiple pesticide residues including insecticides from several chemical
classes in combination with fungicides and less commonly with herbicides. These findings raise
serious concerns about the possible combined effects these chemicals may have on honey bee
health from acute as well as chronic exposures. We are currently investigating the impacts of
these pesticides individually and in combinations on honeybee behavior and survival.
Wax from a broad sampling of brood nests from CCD and other US colonies was also analyzed.
In a total of 88 wax samples analyzed, 20 different pesticides including two of their metabolites
were identified. Figure 3 depicts the 11 most frequently detected pesticide residues in wax and
the percentage of samples found to have the residue. As found in pollen, fluvalinate, coumaphos
and chlorpyrifos were the most commonly detected pesticides with fluvalinate and coumaphos
were detected in 100% of the samples. Amitraz, a compound that breaks down quickly, has not
been detected in any of the samples represented here; however amitraz metabolites have recently
been added to the chemical residues being screened for and have been detected.
lo
os
ni
ul
l
fa
n
(to
ta
l)
Bo
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ic
of
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ot
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or
al
uv
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in
ho
ap
Fl
m
Co
u
n
100
90
80
70
60
50
40
30
20
10
0
s
Percent Frequency (%)
Figure 3. Most frequently detected pesticides in brood nest wax of honey bees.
Pesticides
The problem with fluvalinate
We have always considered fluvalinate a relatively “safe” material for honey bees; however its
history is unclear with potentially significant implications for honey bee health. The original
formulation of fluvalinate (racemic or having multiple forms) had an established lethal dose that
killed 50% of the tested population (LD50) at 65.85 µg/bee for honey bees, which is considered
relatively non-toxic (Atkins et al. 1981). However in the early 1990’s racemic fluvalinate was
replaced with tau-fluvalinate (having a single form) resulting in a 2-fold increase in toxicity of
this material to honey bees. The amended LD50 was then 8.78 µg/bee, a level considered
moderately toxic to honey bees. In addition, US registration of this material changed hands
several times over the past 20 years with potential changes being made in the formulation of
fluvalinate Due in part to the high cost of bringing a pesticide to market, pesticide companies
may make existing pesticides more effective or overcome resistance by changing their chemistry
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or reformulating them. Surprisingly, in 1995 EPA reported the LD50 of fluvalinate as 0.2
µg/bee, a level that is considered to be highly toxic (EPA-OPP 2005) to honey bees. In addition,
Piperonyl butoxide (PBO) (a pesticide synergist often added to formulations of pyrethroids to
increase their potency) can be found in frequent use around urban apiaries. With or without the
addition of PBO or other adjuvants, fluvalinate is now considered to be a highly toxic material to
honey bees. Based on its prevalence in wax, wide-spread resistance in varroa and its toxicity to
honey bees, fluvalinate appears to have outlived is usefulness.
Conclusions
Unprecedented amounts of fluvalinate (up to 204 ppm) at high frequencies have been detected in
brood nest wax, and pollen (bee bread). Changes in the formulation of fluvalinate resulting in a
significant increase in toxicity to honey bees, makes this a serious concern. In addition,
coumaphos, and numerous environmental insecticides along with fungicides and herbicides have
also been widely detected in hive matrices. The large numbers and multiple kinds of pesticides
that have been found could result in potentially toxic interactions for which there are no
scientific studies to date. Europe researchers have found similar pesticides and frequencies in
hive matrices and express similar concerns (Martel et al. 2007). These chronic levels of
pesticides in pollen and wax at potentially acute levels needs to be further investigated with
regard to their potential interactions with other stressors (e.g. IAPV) and their role in CCD. It is
anticipated that additional pesticide analyses of brood, adult bees and nectar samples will provide
valuable insights into recent declines in honey bee health. Figure 4 summarizes our findings and
highlights our major concerns regarding the unknown consequences for honey bee health. A
more detailed report on this work is currently being prepared for publication in a peer-reviewed
scientific journal.
Recommendations
There is growing evidence that a number of factors, including IAPV, pesticides, varroa mites and
other stress factors such as poor nutrition are most likely involved in the overall declining health
of honey bee colonies in the US. However at this time, members of the CCD working team agree
that there are steps that can be taken to help minimize stress on honey bee colonies and to
improve their chances for survival.
1. Monitor and control varroa mite populations using “soft” chemicals. These soft chemicals
include formic acid (Mite-Away II®), Apiguard ®, and Apilife var®.
2. Reduce pathogen and pesticide build-up in combs by regularly culling old comb, recycling
comb and/or irradiation of old comb. This is particularly recommended for dead-out colonies.
3. Fluvalinate should only be used as a material of last resort. Use of off-label products should
NOT be considered.
4. If coumaphos must be used, only the registered product, CheckMite+® should be considered.
5.Communicate with growers where bees are used for pollination to minimize colony exposure
to agricultural-use pesticides. Some pesticide labels permit application during blooming periods,
but this is definitely not the best procedure for honey bee safety, so work with your grower.
6. Monitor and control Nosema disease using fumagillin.
Acknowledgements
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We wish to recognize the significant input of other CCD workgroup members who contributed to
this work especially Jeff Pettis and Dennis vanEngelsdorp and their team members for the
collection of CCD-study samples and review of this article. Thanks also to Jerry Hayes and
Diana Cox-Foster helpful review and input. We must also recognize the critical analytical work
done by Roger Simonds and his team at the NSL. Lastly, we thank the National Honey Board,
the Florida State Beekeepers, the Tampa Bay Beekeepers and the Penn State, College of
Agriculture Sciences, for the financial support that made this work possible.
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